CoChat
Sign Up
Cited by 7Animal Behavior and Welfare StudiesConservation, Ecology, Wildlife EducationAnimal Behavior and Reproduction

The Concept of Agency, Animal Wellbeing, and the Practical Realities of Ex Situ Breeding Programs in Zoos and Aquariums

Open access
Norman, Max, Brando, Sabrina·2024·Journal of Zoological and Botanical Gardens
DOI 10.3390/jzbg5040038
Open this paper in CoChat — free accountOpen PDF

Abstract

Conservation and animal wellbeing are two key goals of the modern zoo and aquarium. In the case of ex situ conservation breeding programs, there is a unique paradox between these concepts; on some occasions, facilities must balance and mitigate arising conflicts between the wellbeing of animals with the goals of the conservation project. Exerting control over the reproductive lives of animals—choosing when and where they breed, whom they breed with, whether breeding is prohibited altogether, and so on—results in an inherent reduction in the animal’s agency. Considering the growing recognition that providing choice and control to animals enhances wellbeing, it is essential to examine how populations and their breeding are managed. The present review presents challenges in supporting agency for animals bred ex situ by thoroughly exploring the practical realities of working with these animals. Various challenges and areas of consideration, including current research directions, suggestions for future practices, and opportunities moving forward, are highlighted. The importance of careful population management in maximising wellbeing, including the inherent dichotomy of the necessity to limit some reproductive autonomy to preserve animal wellbeing while meeting the needs of breeding programs.

AI snapshot

Written from the paper’s full text.

TL;DR

This review examines the inherent tension between ex situ conservation breeding programs and animal agency, arguing that reproductive control reduces agency while choice and control can improve wellbeing and breeding outcomes. It proposes practical considerations for integrating animal-centred choice into population management, mate selection, handling, rearing, and reproductive technologies.

Key findings

  • Conservation breeding inherently limits reproductive agency by controlling whether animals breed, with whom, when, and what happens to young; the authors argue this creates an ethical paradox because choice and control are central to positive wellbeing.
  • Providing mate choice can improve breeding success: giant pandas allowed free mate choice had improved reproductive success, with the effect increased when choice was mutual; scent-preference studies in stripe-faced dunnarts, cheetahs, and harvest mice found greater pair and reproductive success when animals were paired with preferred males.
  • Scent samples can be used to assess mate preference without moving animals; in stripe-faced dunnarts, freezing scent samples for up to 40 days did not impact female scent preference.
  • Assisted reproductive technologies can reduce stressful translocations and mitigate failed pairings, but they deny animals opportunities to express natural courting and reproductive behaviours; the authors also argue facilities should avoid producing surplus animals rather than relying on culling.

Methods

  • Narrative review of practical realities, ethical considerations, and welfare implications of ex situ conservation breeding programs in zoos and aquariums.
  • No new data were collected or created; the paper synthesizes existing literature, examples, and proposed practices, and includes a non-exhaustive framework checklist in Table 1.
  • Main analysis is conceptual and synthetic, covering reproductive choice, mate choice, training and handling, rearing young, holistic wellbeing, and reproductive technologies.

Limitations

  • The paper states that no new data were collected or created and that all content is available within the manuscript; it also states that the Table 1 checklist is “by no means exhaustive.”
  • The text makes evident that several areas are understudied, including impacts of translocations on zoo animals when social groups and caregivers change, personality as a predictor of transfer or pairing outcomes, and ARTs for many endangered species.
  • The text makes evident that testing reproductive technologies is difficult because of small population sizes, limited numbers of breeding individuals, and unique reproductive systems; the authors also disclose affiliations with AnimalConcepts, a consulting company working on animal wellbeing.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.3390/jzbg5040038

Cites

93 of 93 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

39 of 97 cited sources checked · 22 supported · 0 flagged · accuracy not yet measured

  • Premisecitation

    Animals that have recently experienced transport often experience increased physiological stress and other indicators of compromised wellbeing such as behavioural changes.

    “Animals that have recently experienced transport often experience increased physiological stress and other indicators of compromised wellbeing such as behavioural changes [30,31].”
    Quote in the paperNot a substantial claim1 of 2 sources checked
    • cites [30] Hambrecht, 2020, Diurnal variation of salivary cortisol in captive African elephants (Loxodonta africana) under routine management conditions and in relation to a translocation event, Zoo Biol. source

      Section 1.2 says transport is generally associated with increased glucocorticoid levels, supporting the physiological-stress claim. Section 2.2.2 reports arousal and refusal to respond to keepers in one elephant after transport, but does not establish that behavioural changes often occur or that they indicate compromised wellbeing. The Conclusion also describes the study’s post-transport cortisol increase as nonsignificant. (LLM, conf=0.82)

      Experimental — accuracy not yet measured
    • cites [31] Pohlin, 2021, Challenges to animal welfare during transportation of wild mammals: A review (1990–2020), J. Zoo Wildl. Med. source
  • Premisecitation

    Depending on species social style and individual factors, disrupting the social life of an individual or group can be quite significant.

    “Depending on the social style of the species and individual factors such as age, sex, temperament, and previous experiences, disrupting the social life of the individual or group of animals can be quite significant [42,43].”
    Quote in the paperSubstantial claim1 of 2 sources checked
    • cites [42] Radosevich, 2021, The utility of social network analysis for informing zoo management: Changing network dynamics of a group of captive hamadryas baboons (Papio hamadryas) following an introduction of two young males, Zoo Biol. source
    • cites [43] Williams, E., Bremner-Harrison, S., Hall, C., and Carter, A. (2020). Understanding temporal social dynamics in zoo animal management: An elephant case study. Animals, 10. source

      The Introduction says reduced group stability can harm welfare and identifies fission–fusion species as particularly difficult to manage in zoos. The Discussion (section 4.2) also describes possible species-level differences and age-related changes in elephant social dynamics. Our copy does not establish that temperament or previous experiences affect the significance of social disruption, so it supports the general point but not the full list of factors. (LLM, conf=0.84)

      Experimental — accuracy not yet measured
  • Premisecitation

    Many modern animal wellbeing models require animals to live in species-typical social groups and express normal, non-harmful social behaviours.

    “One element of many modern models of animal wellbeing is that animals should be able to live in species-typical social groups and express normal, non-harmful social behaviours.”
    Quote in the paperSubstantial claim1 of 2 sources checked
    • cites [6] Brando, 2018, The 24/7 approach to promoting optimal welfare for captive wild animals, Behav. Proc. source
    • cites [9] Mellor, D.J., Beausoleil, N.J., Littlewood, K.E., McLean, A.N., McGreevy, P.D., Jones, B., and Wilkins, C. (2020). The 2020 Five Domains Model: Including Human-Animal Interactions in Assessments of Animal Welfare. Animals, 10. source

      Section 2.4 says that opportunities for social species to bond and live with familiar conspecifics, and to engage in affiliative behaviours, can enhance welfare. Section 5.1 describes frustration or loneliness when social animals cannot join conspecifics. The paper supports this element of the Five Domains Model, but does not establish that many distinct modern models require species-typical groups or non-harmful social behaviour for animals generally. (LLM, conf=0.83)

      Experimental — accuracy not yet measured
  • Premisecitation

    Birds provided with various supportive infrastructures ranging in location and difficulty as nest sites had multiple choices for where and how to nest.

    “In this study, birds were provided with various supportive infrastructures ranging in location and difficulty as nest sites, providing the animals with multiple choices for where and how they wanted to nest.”
    Quote in the paperNot a substantial claim1 of 1 sources checked
    • cites [63] Greggor, A.L., Vicino, G.A., Swaisgood, R.R., Fidgett, A., Brenner, D., Kinney, M.E., Farabaugh, S., Masuda, B., and Lamberski, N. (2018). Animal welfare in conservation breeding: Applications and challenges. Front. Vet. Sci., 5. source
  • Premisecitation

    Animals managed ex situ for breeding programs are often subject to regular veterinary procedures to monitor reproductive health and collect data for research on reproductive physiology.

    “Animals who are managed ex situ for breeding programs are often subject to regular veterinary procedures to monitor reproductive health and collect valuable data for research on reproductive physiology.”
    Quote in the paperNot a substantial claim1 of 2 sources checked
    • cites [32] Herrick, 2019, Assisted reproductive technologies for endangered species conservation: Developing sophisticated protocols with limited access to animals with unique reproductive mechanisms, Biol. Reprod. source
    • cites [54] Jewgenow, 2017, Research on reproduction is essential for captive breeding of endangered carnivore species, Reprod. Dom. Anim. source

      The Summary (page not available) discusses technologies for assessing fertility and monitoring reproductive status in conservation breeding, and section 3 describes pregnancy monitoring and sample collection in Iberian lynx. The paper does not establish that ex situ animals are often subjected to regular veterinary procedures, or that such procedures routinely collect research data. (LLM, conf=0.84)

      Experimental — accuracy not yet measured
  • May combine two claims. 25
  • Classified as probably not a substantial claim. 16

  • May combine two claims.

    Premisecitation

    Similar personality has been suggested as a predictor for reproductive success in black rhinoceros and giant pandas, and sociality has been found to influence reproductive frequency in cheetahs.

    “Similar personality has been suggested as a predictor for reproductive success in species including black rhinoceros [5] and giant pandas [46], and personality traits such as sociality have been found to influence reproductive frequency in species such as cheetah [52,53].”
    Quote in the paperSubstantial claim2 of 4 sources checked
    • cites [5] Carlstead, 1999, Black rhinoceros (Diceros bicornis) in U.S. zoos: II. Behavior, breeding success, and mortality in relation to housing facilities, Zoo Biol. source
    • cites [46] Shepherdson, 2015, Free mate choice enhances conservation breeding in the endangered giant panda, Nat. Commun. source

      The Results (Mutual mate preference and reproductive performance; page unavailable) link mutual mate preference with higher copulation and cub production in giant pandas. The Discussion says behavioural compatibility is a possible explanation but that the data do not identify the mechanism. The paper does not establish similarity of personality as a predictor; the black-rhinoceros and cheetah claims have separate citations and are not judged here. (LLM, conf=0.86)

      Experimental — accuracy not yet measured
    • cites [52] Wielebnowski, 1999, Behavioral differences as predictors of breeding status in captive cheetahs, Zoo Biol. source
    • cites [53] Razal, 2016, Multifaceted approach to personality assessment in cheetahs (Acinonyx jubatus), Anim. Behav. Cogn. source

      The Results (page unavailable) report that cheetahs that had reproduced scored higher on the Unsociable personality component. But the study defined reproductive success as having produced at least one litter, not reproductive frequency, and the association does not establish that sociality caused a change in reproduction. The rhinoceros and panda claims have separate citations and are not assessed here. (LLM, conf=0.87)

      Experimental — accuracy not yet measured

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Ultrasound scans and sample collection are typical procedures for animals in breeding programs.

    “Ultrasound scans and sample collection are typical procedures [32,54].”
    Quote in the paperNot a substantial claim1 of 2 sources checked
    • cites [32] Herrick, 2019, Assisted reproductive technologies for endangered species conservation: Developing sophisticated protocols with limited access to animals with unique reproductive mechanisms, Biol. Reprod. source
    • cites [54] Jewgenow, 2017, Research on reproduction is essential for captive breeding of endangered carnivore species, Reprod. Dom. Anim. source

      Section 3 (page unavailable) describes collecting blood, urine and faecal samples to monitor pregnancy in a conservation breeding programme, supporting the sample-collection part. The only ultrasound mention found is in a reference title; the paper does not establish that ultrasound scans are typical procedures in breeding programmes. (LLM, conf=0.85)

      Experimental — accuracy not yet measured

  • May combine two claims.

    Premisecitation

    Personality has been suggested as a method of determining group compatibility, but more evidence is needed to implement it effectively for predicting transfer outcomes or pairing success.

    “Personality has been suggested as one method of determining group compatibility [44]; however, there is a need for more evidence to implement personality effectively as a tool for predicting outcomes of transfers or whether a pairing is likely to be successful.”
    Quote in the paperNot a substantial claim1 of 1 sources checked
    • cites [44] Norman, 2021, Potential applications of personality assessments to the management of non-human primates: A review of 10 years of study, PeerJ source

  • May combine two claims.

    Premisecitation

    Culling animals that are not considered genetically valuable is already commonplace and is regarded by many facilities as a routine and normal aspect of managing breeding populations.

    “Culling animals that are not considered genetically valuable is already commonplace and is regarded by many facilities as a routine and normal aspect of managing breeding populations [68].”
    Quote in the paperSubstantial claim1 of 1 sources checked
    • cites [68] Browning, 2018, No Room at the Zoo: Management euthanasia and animal welfare, J. Agri. Environ. Ethics source

      The Introduction says that animals from well-represented genetic lines can be surplus to breeding requirements and that management euthanasia of healthy surplus animals is relatively common in European zoos. It does not establish that many facilities regard culling as a routine and normal practice; the paper also describes debate over its acceptability. (LLM, conf=0.84)

      Experimental — accuracy not yet measured

  • May combine two claims.

    Premisecitation

    Contraception may be used to modify undesirable social behaviour, manage reproductive system health, and improve wellbeing by maintaining social groups and reducing pregnancy and rearing demands.

    “Different forms of contraception may also be considered for goals such as modifying undesirable social behaviour, such as testosterone-related aggression (antelopes [16]; elephants [17]; primates: [18])”
    Quote in the paperNot a substantial claim1 of 3 sources checked
    • cites [16] Penfold, 2002, Case studies in antelope aggression using a GnRH agonist, Zoo Biol. source
    • cites [19] Asa, 2013, Factors Associated with Uterine Endometrial Hyperplasia and Pyometra in Wild Canids: Implications for Fertility, Zoo Biol. source
    • cites [14] Cronin, 2016, Investigating the relationship between welfare and rearing young in captive chimpanzees (Pan troglodytes), App. Anim. Behav. Sci. source

      The Introduction describes contraception of female chimpanzees to interrupt reproductive cycling, and the Conclusions address whether rearing young benefits their welfare. The copy does not address using contraception to modify testosterone-related aggression or other undesirable social behaviour in primates; searches for those terms found only a definition of self-aggression, not a finding about contraception. (LLM, conf=0.75)

      Experimental — accuracy not yet measured

  • May combine two claims.

    Premisecitation

    The reproductive strategy of an animal varies by species, including female choice or rejection, male selection, and coercive strategies.

    “The reproductive strategy of an animal varies depending on the species; for example, in some animals, the female chooses or rejects the males (striped-faced dunnarts Sminthopsis macroura [23]), [24] while in others, males select the females [25] sometimes using coercive strategies [13].”
    Quote in the paperNot a substantial claim1 of 3 sources checked
    • cites [23] Parrott, 2019, Female mate choice significantly increases captive breeding success, and scents can be frozen to determine choice, in the stripe-faced dunnart, Appl. Anim. Behav. Sci. source
    • cites [25] Keagy, 2019, Sex differences in cognition and their relationship to male mate choice, Current Zool. source
    • cites [13] Kunz, 2021, The context of sexual coercion in orang-utans: When do male and female mating interests collide?, Anim. Behav. source

  • May combine two claims.

    Premisecitation

    In the wild, individuals of many social species disperse from their natal group to find and select a mate in a different group or live solitary with overlapping territories.

    “In the wild, individuals of many social species will disperse from their natal group to find and select a mate in a different group or live a solitary life where their territory may overlap with those of potential mates [29].”
    Quote in the paperNot a substantial claim1 of 1 sources checked
    • cites [29] Li, X.Y., and Kokko, H. (2019). Intersexual resource competition and the evolution of sex-biased dispersal. Front. Ecol. Evo., 7. source

      The Introduction (page unavailable) describes offspring leaving their natal site, and the Methods (page unavailable) model dispersal between sites where individuals compete for breeding positions and mate. The paper does not establish the claim about many social species in the wild, mate selection in a different group, or solitary individuals whose territories overlap with potential mates. (LLM, conf=0.85)

      Experimental — accuracy not yet measured

  • May combine two claims.

    Premisecitation

    Some primary concerns in managed breeding programs are a lack of fulfilled recommendations or many pairs that do not successfully reproduce despite relocation and pairing efforts.

    “Some primary concerns are a lack of fulfilled recommendations or many pairs that do not successfully reproduce despite efforts to relocate and bring pairs together for breeding [4].”
    Quote in the paperNot a substantial claim1 of 1 sources checked
    • cites [4] Gray, 2021, Reasons for unfulfilled breeding and transfer recommendations in zoos and aquariums, Zoo Biol. source

  • May combine two claims.

    Premisecitation

    Giant pandas allowed to choose their mates freely had improved reproductive success, and this effect was increased when the choice was mutual.

    “For example, giant pandas (Ailuropoda melanoleuca) who were allowed to choose their mates freely had improved reproductive success, and this effect was increased when the choice was mutual between both members of the pairing [46].”
    Quote in the paperSubstantial claim1 of 1 sources checked
    • cites [46] Shepherdson, 2015, Free mate choice enhances conservation breeding in the endangered giant panda, Nat. Commun. source

  • Classified as probably not a substantial claim.

    Premisecitation

    Personality might be linked to certain social measures critical to reproductive success.

    “Seyfarth et al. suggest that personality might be linked to certain social measures critical to reproductive success [50], while Powell and Gartner suggest that personality may have a role in mate selection [51].”
    Quote in the paperSubstantial claim1 of 2 sources checked
    • cites [50] Seyfarth, 2012, Variation in personality and fitness in wild female baboons, Proc. Natl. Acad. Sci. USA source
    • cites [51] Powell, D., and Gartner, M. (2011). Applications of personality to the management and conservation of nonhuman animals. From Genes to Animal Behavior: Primatology Monographs, Springer. source

  • Classified as probably not a substantial claim.

    Premisecitation

    A holistic animal wellbeing program includes access to appropriate nutrition, positive emotions, reduced negative emotions, and species-typical behaviours.

    “A holistic animal wellbeing program includes access to appropriate nutrition, experiencing positive emotions, reducing negative emotions, and performing species-typical behaviours [6,9].”
    Quote in the paperSubstantial claim1 of 2 sources checked
    • cites [6] Brando, 2018, The 24/7 approach to promoting optimal welfare for captive wild animals, Behav. Proc. source
    • cites [9] Mellor, D.J., Beausoleil, N.J., Littlewood, K.E., McLean, A.N., McGreevy, P.D., Jones, B., and Wilkins, C. (2020). The 2020 Five Domains Model: Including Human-Animal Interactions in Assessments of Animal Welfare. Animals, 10. source

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Some species live in family groups with one breeding pair, while others live in multi-male or multi-female harems.

    “Some species live in family groups with one breeding pair (canids [26]), while other species may live in multi-male or multi-female harems (ungulates [27]; primates [28]).”
    Quote in the paperNot a substantial claim2 of 3 sources checked
    • cites [26] Vonk, J., and Shackelford, T.K. (2019). Canine life history. Encyclopedia of Animal Cognition and Behavior, Springer. source
    • cites [27] Bowyer, 2020, Evolution of ungulate mating systems: Integrating social and environmental factors, Ecol. Evol. source
    • cites [28] Xia, W., Grueter, C.C., Ren, B., Zhang, D., Yuan, X., and Li, D. (2021). Determinants of harem size in a polygynous primate: Reproductive success and social benefits. Animals, 11. source

  • May combine two claims.

    Premisecitation

    Mother-young bonds are essential to proper psychosocial development in many species, and unnecessary early separation is detrimental to normal development and the wellbeing of both individuals.

    “Such bonds are essential to proper psychosocial development in many species [71] and unnecessary early separation is thus detrimental to both normal development and the wellbeing of both individuals.”
    Quote in the paperSubstantial claim1 of 1 sources checked
    • cites [71] Broad, 2006, Mother-infant bonding and the evolution of mammalian social relationships, Philos. Trans. R. Soc. Lond. B. Biol. Sci. source

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Many have put forth ethical and moral arguments against culling surplus animals.

    “Many have put forth similar ethical and moral arguments against culling surplus animals [68,69].”
    Quote in the paperNot a substantial claim2 of 2 sources checked
    • cites [68] Browning, 2018, No Room at the Zoo: Management euthanasia and animal welfare, J. Agri. Environ. Ethics source
    • cites [69] Pierce, 2018, A postzoo future: Why welfare fails animals in zoos, J. Appl. Anim. Welf. Sci. source

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    A simple puzzle can allow animals to decide when to forage by only releasing food when the puzzle is completed.

    “Enrichment, for example, can provide additional complexity in a habitat; a simple puzzle can allow animals to decide when to forage by only releasing food when the puzzle is completed [77].”
    Quote in the paperNot a substantial claim1 of 1 sources checked
    • cites [77] Krebs, 2017, Simple but temporally unpredictable puzzles are cognitive enrichment, Anim. Behav. Cogn. source

      The Discussion (page not provided) says the rhino could choose whether to respond to the feeder’s cue, supporting the claim that the puzzle gave him some control over when to forage. The Puzzle Feeder Mechanism section says food compartments opened on a timed or remotely controlled schedule; the rhino then had to roll the ball to extract food. Food availability therefore did not depend solely on completing the puzzle. (LLM, conf=0.86)

      Experimental — accuracy not yet measured

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    The One Plan Approach and One Conservation emphasise improving all aspects of managing populations, including developing new technologies that safeguard animal wellbeing in the wild and human care while maintaining genetically healthy populations.

    “These approaches emphasise improving all aspects of managing populations, including developing new technologies that safeguard animal wellbeing in the wild and human care while maintaining genetically healthy populations.”
    Quote in the paperNot a substantial claim1 of 1 sources checked
    • cites [94] Pizzutto, 2021, One Conservation: The integrated view of biodiversity conservation, Anim. Reprod. source

      Split into 2 atoms — 0 confirmed, 2 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.

      Experimental — accuracy not yet measured

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    The need for integration between ex situ and in situ population management and the expansion of technologies through research is highlighted by the International Union for the Conservation of Nature's One Plan Approach and further through the lens of One Conservation.

    “The need for integration between ex situ and in situ population management and the expansion of technologies through research is highlighted by the International Union for the Conservation of Nature's (IUCN) One Plan Approach (OPA), and further through the lens of One Conservation [94].”
    Quote in the paperNot a substantial claim1 of 1 sources checked
    • cites [94] Pizzutto, 2021, One Conservation: The integrated view of biodiversity conservation, Anim. Reprod. source

  • May combine two claims.

    Interpretationreasoning

    In cases where young are abandoned or parents are ineffective, alloparenting by a suitable alternative parent of the same species may be possible, but not in all cases, particularly for solitary species.

    “It may be the case that there is a suitable alternative parent of the same species other than the biological mother, and alloparenting may be possible.However, this is not possible in all cases, particularly when discussing solitary species.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationreasoning

    Introducing animals even briefly to test compatibility can be stressful and pose potential health and safety risks to all animals involved.

    “Thirdly, introducing animals-even if only to see if they are compatible briefly-can be stressful and pose potential health and safety risks to all animals involved, as discussed earlier.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    There is much evidence of zoos successfully implementing various contraceptive methods.

    “However, there is much evidence of zoos' successful implementation of various methods [20][21][22].”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [20] Agnew, 2016, A review of population control methods in captive-housed primates, Anim. Welf. source
    • cites [21] Patton, 2007, Review of contraception in ungulate species, Zoo Biol. source
    • cites [22] Comizzoli, P., Brown, J.L., and Holt, W.V. (2019). Fertility Control in Wildlife: Review of Current Status, Including Novel and Future Technologies. Reproductive Sciences in Animal Conservation, Springer. source

  • May combine two claims.

    Premisecitation

    Many wild species do not have successful or well-studied methods for artificial insemination, meaning animals must be brought together for breeding in most cases.

    “Many wild species do not have successful or well-studied methods for artificial insemination [32] which means animals must be brought together for breeding in most cases.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [32] Herrick, 2019, Assisted reproductive technologies for endangered species conservation: Developing sophisticated protocols with limited access to animals with unique reproductive mechanisms, Biol. Reprod. source

  • May combine two claims.

    Premisecitation

    Forceful and coercive handling methods are stressful, and chemical restraint without effective positive reinforcement training beforehand is stressful and frightening from the animal's perspective.

    “For example, it is well known that forceful and coercive handling methods are stressful [55,56] and that chemical restraint without effective positive reinforcement training beforehand is stressful and frightening from the animal's perspective.”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [55] Hurst, 2010, Taming anxiety in laboratory mice, Nat. Methods source
    • cites [56] Uetake, 2002, Flight distance of dairy cows and its relationship to daily routine management procedures and productivity, Anim. Sci. J. source

  • May combine two claims.

    Interpretationnone given

    Introducing animals for any purpose, including breeding, is risky; there is no guarantee of compatibility beyond genetics, and there is always a risk of injury and death during introductions.

    “Moreover, introducing animals for any purpose, including breeding, is risky.There is no guarantee that animals will be compatible beyond genetics, and there is always a risk of injury and even death during introductions.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based). May combine two claims.

    Interpretationnone given

    Best practices today for human intervention in rearing include feeding practices that briefly remove the young from the group, feeding the young while in the group and held by the mother or other group members, or housing the young with conspecifics next to the group to maintain social contact.

    “Best practices today include bottle or other feeding practices that briefly remove the young from the group, feeding the young while they are in the group and held by the mother or other group members, or housing the young with conspecifics next to the group to be able to feed and also maintain social contact.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation

    The aims of contraception in managed breeding include managing genetic composition, reducing inbreeding, and modifying generation length.

    “The aims of contraception are variable: to manage the population's genetic composition, reduce inbreeding, and modify generation length as the primary concerns [15].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [15] Lacy, 2012, Achieving true sustainability of zoo populations, Zoo Biol. source

  • May combine two claims.

    Interpretationnone given

    It is neither feasible nor conducive to animal welfare to transport all potential mates to one site for animals to choose from.

    “Firstly, it is neither feasible nor conducive to animal welfare to transport all potential mates to one site for the animals to choose from.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationcitation

    The process of translocation exerts multiple negative stressors, including capture and restraint, confinement during transport, and release in an unfamiliar environment with unfamiliar animals and care staff.

    “The process of translocation exerts multiple negative stressors, including capture and restraint for transport if animals are not trained to participate voluntarily, confinement during the transport process, which may be by land, sea, or air, and eventual release in an unfamiliar environment, to unfamiliar animals and unfamiliar care staff.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S4 (based).

    Interpretationnone given

    Occasionally, animals may not be effective at parenting their young, particularly first-time parents without prior experience.

    “Occasionally, animals may not be effective at parenting their young-particularly for first-time parents without prior experience.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S2 (checkable), S4 (based).

    Interpretationnone given

    Exerting control over the reproductive lives of animals results in an inherent reduction in the animal's agency.

    “Exerting control over the reproductive lives of animals-choosing when and where they breed, whom they breed with, whether breeding is prohibited altogether, and so on-results in an inherent reduction in the animal's agency.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S4 (based).

    Interpretationnone given

    Allowing animals to freely mate with whomever they choose may not be in the best interests of the whole population's genetic health.

    “Secondly, allowing animals to freely mate with whomever they choose may not be in the best interests of the whole population's genetic health.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S2 (checkable), S4 (based). May combine two claims.

    Interpretationreasoning

    With sufficient choice, control, and attention to wellbeing, the needs of conservation breeding programs can be met while promoting a positive quality of life throughout the lifespan of mothers, fathers, youngsters, and all other animals.

    “With sufficient choice, control, and attention to wellbeing, the needs of conservation breeding programs can be met while promoting a positive quality of life throughout the lifespan of mothers, fathers, youngsters, and all other animals.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationreasoning

    Of the individuals considered in ex situ programs, only a small number will be considered for potentially invasive trials of assisted reproductive technologies for some species, and experimentation with various technologies may not be possible under current conditions.

    “Of those individuals, only a small number will be considered for potentially invasive trials of ARTs for some species, and experimentation with various technologies may not be possible under current conditions.”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: Only viable individuals—i.e., those cared for under optimal conditions for wellbeing—are to be considered in ex situ programs.

  • May combine two claims.

    Premisecitation

    Trials of artificial insemination in rhinoceros have been successful, presenting a possible option for producing viable offspring and restoring genotypes that had been lost.

    “Trials of artificial insemination in rhinoceros have been successful, presenting a possible option for producing viable offspring and restoring genotypes which had been lost [87].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [87] Hermes, 2009, First successful artificial insemination with frozen-thawed semen in rhinoceros, Theriogenology source

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationnone given

    Financial or other resource constraints on zoos do not mean opportunities to implement choice and control are unavailable.

    “Of course, many zoos are limited in their ability to implement specific technology due to financial or other resource constraints; this does not mean opportunities to implement choice and control are unavailable.”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: Many zoos are limited in their ability to implement specific technology due to financial or other resource constraints.

  • Probably not a substantial claim: may not pass S2 (checkable), S4 (based).

    Interpretationreasoning

    By understanding the mechanisms by which animals select mates and what qualities influence the likelihood of pair success in a wide variety of managed species, caregivers and those responsible for managing breeding programs can make more informed choices about breeding recommendations and the pairings which are likely to be both successful and beneficial to the wellbeing of the animals.

    “By understanding the mechanisms by which animals select mates and what qualities influence the likelihood of pair success in a wide variety of managed species, caregivers and those responsible for managing breeding programs can make more informed choices about breeding recommendations and the pairings which are likely to be both successful and beneficial to the wellbeing of the animals.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation

    Semen and other materials can be stored and transported over long distances, reducing the need to transfer animals across long distances for breeding purposes.

    “Semen and other materials can be stored and transported over long distances [92], reducing the need to transfer animals across long distances for breeding purposes.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [92] Durrant, 2009, The importance and potential of artificial insemination in CANDES (companion animals, non-domestic, endangered species), Theriogenology source
36 of 36

  • The paper relies on this without support.

    Conservation and animal wellbeing are two key goals of modern zoos and aquariums.

    “Conservation and animal wellbeing are two key goals of the modern zoo and aquarium.”

  • The paper relies on this without support.

    For many endangered species of zoo-housed wild animals, carefully managed breeding programs are an essential element of conservation work at these facilities.

    “For many endangered species of zoo-housed wild animals, carefully managed breeding programs are an essential element of the conservation work at these facilities.”

  • The paper relies on this without support.

    Human caregivers can make informed reproductive decisions based on science, ethics, and empathy for the animals.

    “Human caregivers can make an informed decision based on science, ethics, and empathy for the animals.”

  • The paper relies on this without support.

    Animals in the wild and in human care may not necessarily make optimal choices for their wellbeing or the wellbeing of their young.

    “Animals in the wild and, indeed, in human care may not necessarily make optimal choices for their wellbeing or the wellbeing of their young.”

  • The paper relies on this without support.

    A positive outcome for the whole population from transferring an animal for breeding outweighs the compromise on animal wellbeing.

    “For example, while translocations and introductions are stressful for animals, a positive outcome for the whole population from transferring that animal for breeding outweighs the compromise on animal wellbeing.”

  • The paper relies on this without support.

    Many zoos are limited in their ability to implement specific technology due to financial or other resource constraints.

    “Of course, many zoos are limited in their ability to implement specific technology due to financial or other resource constraints; this does not mean opportunities to implement choice and control are unavailable.”

  • The paper relies on this without support.

    Only viable individuals—i.e., those cared for under optimal conditions for wellbeing—are to be considered in ex situ programs.

    “Only viable individuals-i.e., those cared for under optimal conditions for wellbeing-are to be considered in ex situ programs.”
7 of 7

Cites

Flagged first, then by citations

Research works printed but not linked: 4

  1. Jachowski, 2009, Reintroducing the black-footed ferret Mustela nigripes to the Great Plains of North America, Small Carniv. Conserv., 41, 58
  2. Wood, 2013, Evaluation of fission-fusion in spider monkeys at the Little Rock Zoo, J. Contents, 18, 15
  3. Kastelein, 1995, Improving parental care of a female bottlenose dolphin (Tursiops truncates) by training, Aquat. Mamm., 21, 165
  4. Brando, S. (2018, January 30). Promoting optimal animal welfare in population management programs. Proceedings of the WAZA Committee for Population Management, 3rd Joint TAG Chairs Meeting, Budapest Zoo and Botanical Gardens, Budapest, Hungary.

Cited by

Sorted by citations

Related

Authors
Norman, M., & Brando, S.
Affiliations
AnimalConcepts, Teulada, 03725 Alicante, Spain
Corresponding author
Brando, Sabrina
ORCID
Venue
Journal of Zoological and Botanical Gardens
Publisher
MDPI AG
Published
2024-09-30
Volume
5
Issue
4
Pages
563-578
ISSN
2673-5636 (ISSN-L)
DOI
10.3390/jzbg5040038
OpenAlex
W4402965832
Semantic Scholar
907e653932e26a4d022e0fd0da89b60a357664dc
Cited by
7
References
92
Citations by year
2026: 4 · 2025: 3
FWCI
3.36
Type
journal article
Language
en
Update notices
correction (2024-09-30)
Open access
Licence
Locations
  • Journal of Zoological and Botanical Gardens (publishedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Topics
  • Health Sciences › Veterinary › Small Animals › Animal Behavior and Welfare Studies
  • Physical Sciences › Environmental Science › Management, Monitoring, Policy and Law › Conservation, Ecology, Wildlife Education
  • Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
Keywords
animal agency, animal welfare, ex situ conservation, captive breeding programs, zoo animals, aquarium animals, reproductive autonomy, population management, captive breeding

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Claims read by deepseek-v4.1-flash under definition version 3 (extract-v3) on 2026-10-28.

Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-10-28.

Cited sources are checked by gpt-6-sol.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review